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Cestoda: Caryophyllidea): Karyotype and Localization of Telomeric and Ribosomal Sequences After Fluorescence in Situ Hybridization (FISH)

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Cestoda: Caryophyllidea): Karyotype and Localization of Telomeric and Ribosomal Sequences After Fluorescence in Situ Hybridization (FISH) Parasitology Research (2019) 118:2789–2800 https://doi.org/10.1007/s00436-019-06450-3 FISH PARASITOLOGY - ORIGINAL PAPER Chromosomal study of Khawia abbottinae (Cestoda: Caryophyllidea): karyotype and localization of telomeric and ribosomal sequences after fluorescence in situ hybridization (FISH) Martina Orosová1 & Irena Provazníková2,3 & Bing Wen Xi4 & Mikuláš Oros1 Received: 17 June 2019 /Accepted: 28 August 2019 /Published online: 4 September 2019 # Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract An original cytogenetic study combining classical karyotype analysis and modern fluorescence in situ hybridization using telomeric (TTAGGG)n and ribosomal sequences (18S rDNA) was performed in Khawia abbottinae (Cestoda, Caryophyllidea), a parasite of Chinese false gudgeon (Abbottina rivularis) from China. Analyses based on conventional Giemsa staining, DAPI, YOYO-1 dye, and silver (Ag) staining were also carried out. The karyotype is composed of eight pairs of metacentric and telocentric chromosomes (2n =16, n=5m +3t). Constitutive heterochromatin was mainly positioned at pericentromeric regions, and telomeric sequences (TTAGGG)n were restricted to the end of all chromosomes. In mitotic preparations stained with Giemsa, both homologues of chromosome pair 4 showed a distinct secondary constriction. FISH with rDNA probe confirmed that this secondary constriction contains a nucleolar organizer region (NOR). The process of spermatocyte meiosis and the dynamics of nucleolus degradation in dividing cell were scrutinized. The present study and its results enhance the limited knowledge on basic karyotype characteristics and 18S rDNA clusters location in caryophyllidean tapeworms. Keywords Cestoda . Karyotype . FISH . 18S rDNA mapping . Telomeres Introduction one set of reproductive organs (Mackiewicz 1994). Recent studies revealed several unusual molecular and genetic phe- Tapeworms of the order Caryophyllidea represent a unique nomena (Kráľová-Hromadová et al. 2012;Brabecetal.2012; group among the “true” cestodes (Eucestoda) in that they are Scholz et al. 2014; Hanzelová et al. 2015; Špakulová et al. monopleuroid, i.e. their body is monozoic and contains only 2019), such as the lineage-specific nuclear paralogs of mtDNA, intraindividual divergence of ribosomal internal tran- scribed spacers 2 (ITS2) along with multiple rDNA loci, cryp- Handling Editor: Julia Walochnik tic species diversity, phenotypic variability but genetic unifor- mity, and the triploid character of some species. Knowledge * Martina Orosová [email protected] on the chromosome sets of caryophyllidean tapeworms is rather scanty; thus far, 23 tapeworm species have been studied cytogenetically, and the karyotypes complements of only 14 1 Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, species have been recognized in all details (for a review, see 040 01 Košice, Slovakia Špakulová et al. 2011; Orosová and Oros, 2012). 2 š Institute of Entomology, Biology Centre CAS, Brani ovská 31, 370 The genus Khawia Hsü, 1935, the most specious genus of 05 České Budějovice, Czech Republic the order Caryophyllidea, contains eight valid species parasit- 3 Č Faculty of Science, University of South Bohemia in eské izing cyprinid fishes with worldwide distribution, except for Budějovice, Branišovská 1760, 370 05 České Budějovice, Czech Republic the neotropical region (Scholz et al. 2011; Scholz and Oros 2017). Khawia abbottinae Xi, Oros, Wang, Scholz and Xie, 4 Key Laboratory of Freshwater Fisheries and Germplasm Resources Utilization, Ministry of Agriculture, Freshwater Fisheries Research 2013 was originally described as a specific parasite of the Center, Chinese Academy of Fishery Sciences, Wuxi 214081, China Chinese false gudgeon, Abbottina rivularis (Cyprinidae, 2790 Parasitol Res (2019) 118:2789–2800 Gobioninae), from the Yangtze River basin in China (Xi et al. ribosomal genes. Additionally, FISH with the telomeric probe 2013). In total, the authors reported five species of the genus (TTAGGG)n was performed to the examined karyotype for Khawia (K. abbottinae, K. japonensis, K. rossittensis, thepossiblepresenceofinterstitial telomeric sequences K. saurogobii and K. sinensis) in China. (ITS). Moreover, the present study also focused on a descrip- Within the family Lytocestidae, chromosomes have been tion of heterochromatin distribution (DAPI-banding) and the studied only sparsely and the knowledge of karyotype organi- occurrence of nucleoli during meiosis by staining with fluo- zation has been limited to 6 species of 3 genera to date (for rescent dye YOYO-1. review see Špakulová et al. 2011; Orosová and Oros 2012). The majority of previous studies were based exclusively on a description of the diploid number, with low emphasis on chro- Materials and methods mosome morphology. For the genus Khawia, karyological analysis of 4 species, namely K. japonensis (under synonym Specimens of K. iowensis, Grey 1979), K. sinensis, K saurogobii and K. rossittensis revealed a constant diploid number, 2n =16, Fifteen alive specimens of Khawia abbottinae were obtained and similar chromosome morphology (Grey 1979; from the intestine of the Chinese false gudgeon (Abbottina Petkevičiūtė 1998; Mutafova and Nedeva 1999;Orosová rivularis) from water bodies of the middle and lower reaches et al. 2010a; Orosová and Oros 2012). Repetitive DNA anal- of the Yangtze River basin (Yangtze River in Wuhan, Hubei ysis has shown only a very low variation in the arrangement of province, and Taihu Lake in Wuxi, Jiangsu province) in April heterochromatin along the chromosomes among the studied 2011 and April 2018. Tapeworms were dissected from the species. Thus, it is difficult to identify chromosome rearrange- intestine of freshly killed fish, rinsed several times in saline ments and to study chromosome evolution within this genus solution, and processed immediately for chromosome slide based on classical karyotype analysis. Ribosomal DNAs are preparations, and subsamples of specimens were fixed in valuable cytogenetic markers in plant and animal genome re- 96% ethanol for DNA extraction. search, as they are presented in numerous repeated units, gen- erally organized in clusters, and thus are easily visualized in Chromosome preparations the chromosomes. Fluorescent in situ hybridization (FISH) has been used for decades for physical mapping of repeated For cytogenetic analysis, whole living tapeworms were incu- sequences, such as ribosomal DNAs on mitotic and meiotic bated in 0.025% colchicine solution (in saline) for 1 h at room chromosomes in various organisms (Nguyen et al. 2010; temperature (RT). Thereafter, they were placed into a hypo- Sheng and Wang 2010; Cabral-de-Mello et al. 2011; tonic solution of 0.75 M KCl for 2 h at RT and torn gently at Bombarová et al. 2015; Solovyeva et al. 2016; Teixeira et al. the testicular body area using the insulin syringes. The torn 2017;Supiwongetal.2019). There are rarely any molecular worms were placed into freshly prepared cold fixative solution cytogenetic studies that use FISH to map the ribosomal genes (methanol to acetic acid, 3:1) with two changes, 15 min each. of caryophyllidean tapeworms, and such data are available for The fixed material was stored at − 20 °C. only four species. In the genus Khawia, a single locus bearing Spread chromosome preparations were made using the a nuclear organizer region (NOR) was detected at the homo- method according to Orosová and Špakulová (2018). logues of pair 7 in K. saurogobii and of pair 6 in K. sinensis Shortly, small pieces containing medullary parenchyma with (Orosová et al. 2010a; Orosová and Oros 2012). In both spe- testes were transferred into a drop of 60% acetic acid on a cies, FISH with the 18S rDNA probe identified major rDNA clean slide and torn into fine pieces with the help of tungsten clusters located in the pericentromeric region on the small needles. The slide was then placed on a heating plate at 45 °C, metacentric chromosome. and the drop of cell suspension was slowly drawn along the Cytogenetic studies can contribute an array of information slide until the liquid evaporated. The preparations were passed independent from morphological and molecular characteris- through an ethanol series (70, 80, and 100%, 1 min each) and tics, which are routinely used for phylogenetic analysis. The stored at − 20 °C until further use. Before each kind of stain- differences and similarities may not be apparent at the molec- ing, preparation was removed from the freezer, dehydrated in ular or morphological level. However, they could be revealed an ethanol series, and air-dried. through karyological data (Sessions 1996). The intention of the current work was to extend the limited knowledge of chro- Karyological analysis mosomes in caryophyllidean tapeworms. An in-depth chro- mosomal analysis (number, size, morphology) in a newly de- The preparations were stained with 5% solution of Giemsa scribed species of the family Lytocestidae, K. abbottinae,was (Merck, NJ, USA) in phosphate buffer (pH 6.8) for 25 min carried out for the first time. Number and location of NORs and rinsed with distilled water. Detailed analysis (length, mor- were analysed through Ag staining and FISH with 18S phology and centromeric index of chromosomes) was Parasitol Res (2019) 118:2789–2800 2791 performed in 10 best mitotic spreads (with clearly distinguish- DNA polymerase I (ThermoFisher, Waltham, MA, USA). able chromosomes) out of 112 evaluated dividing cells from 9 The reaction time was 1 h at 15 °C. worms. The chromosomes
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